Nutrient Uptake Changes in Ascorbate Free Radical-Stimulated Onion Roots

González‐Reyes, José A.; Hidalgo, Antonio; Caler, J. A.; Palos, R.; Navas, Plácido

doi:10.1104/pp.104.1.271

Cited by 49 publications

(22 citation statements)

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“…ASC is a common compound in plants that may be physiologically involved in the regulation of cell-wall extensibility. Our group has published a number of observations that indicate that ASC and its free radical stimulate root elongation and accelerate the quiescence-proliferation transit in onion roots (Hidalgo et al, 1991;De Cabo et al, 1993;González-Reyes et al, 1994b), and similar results are shown in this paper. Onions grown in the presence of ASC had significantly longer roots than onions grown in control conditions; however, DHA inhibited cell elongation, supporting our previously reported data (González-Reyes et al, 1994a).…”

Section: Discussionsupporting

confidence: 86%

“…On the other hand, ASC or CL treatments decreased both apoplast and cell-wall-bound peroxidase activities, whereas Lyc had a slight stimulating effect. These results are discussed on the basis of a possible control of root elongation by ASC via its action on peroxidases that are involved in the regulation of cell-wall extensibility.ASC and its free radical AFR stimulate the elongation of onion (Allium cepa L.) roots in parallel to a high vacuolization of meristematic cells (Hidalgo et al, 1989;Navas, 1991;González-Reyes et al, 1994b). ASC is required for the progression of the G1 and G2 phases of the cell cycle (Liso et al, 1984).…”

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“…ASC and its free radical AFR stimulate the elongation of onion (Allium cepa L.) roots in parallel to a high vacuolization of meristematic cells (Hidalgo et al, 1989;Navas, 1991;González-Reyes et al, 1994b). ASC is required for the progression of the G1 and G2 phases of the cell cycle (Liso et al, 1984).…”

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Role of Apoplastic and Cell-Wall Peroxidases on the Stimulation of Root Elongation by Ascorbate

et al. 1996

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Elongation of onion (Allium cepa L.) roots was highly stimulated by ascorbate (ASC) and its natural precursor I-galactone-y-lactone (CL). When incubation media were supplemented with lycorine (Lyc), an inhibitor of the ASC biosynthesis, root growth was negligible even in the presence of ASC or CL. ASC completely inhibited in vitro guaiacol peroxidase activities that were isolated from both the apoplast and the cell wall. However, ferulic-acid-dependent peroxidase from the cell wall was partially inhibited by ASC, whereas ferulic acid peroxidase activity from the apoplastic fluid was completely inhibited by ASC as long as ASC was present in the assay medium. ASC content in cells was increased by preincubations with ASC or CL, whereas Lyc reduced it. On the other hand, ASC or CL treatments decreased both apoplast and cell-wall-bound peroxidase activities, whereas Lyc had a slight stimulating effect. These results are discussed on the basis of a possible control of root elongation by ASC via its action on peroxidases that are involved in the regulation of cell-wall extensibility.ASC and its free radical AFR stimulate the elongation of onion (Allium cepa L.) roots in parallel to a high vacuolization of meristematic cells (Hidalgo et al., 1989;Navas, 1991;González-Reyes et al., 1994b). ASC is required for the progression of the G1 and G2 phases of the cell cycle (Liso et al., 1984). Current explanations for these observations include (a) the hyperpolarization of the plasma membrane and acidification of the apoplast induced by ASC and AFR (González-Reyes et al., 1992) after the activation of a plasmalemma NADH-AFR oxidoreductase activity that stimulates nutrient intake (Gonzalez-Reyes et al., 1994b), and (b) the maintenance, in a reduced state of Hyp-rich proteins, that is needed for the progression of the cell cycle (Arrigoni et al., 1977;De Gara et al., 1991a). Two recent reviews analyze these hypotheses in detail (Arrigoni, 1994; Cór-doba and González-Reyes, 1994).Root growth and elongation leads to an irreversible increase in cell volume. Thus, the cell-wall architecture is modified in such a way that a relaxation of the crossed bonds that link severa1 components of the cell wall must 95-0560).occur. Cell-wall loosening allows the increase of the cell surface and the intake of water by the protoplast, and changes in the cell-wall architecture during cell elongation have been recently reported (McCann and Roberts, 1994). Cell-wall-bound and/ or apoplastic peroxidases have been involved in the formation of isodityrosine bonds between glycoproteins as extensin, or diferulate bridges between polysaccharide polymers (Biggs and Fry, 1987). These peroxidase-driven cross-linking reactions of cellwall polymers stiffened the cell wall during growth, thus reducing the rate of elongation (Fry, 1986). To comprehend the regulation of cell-wall extensibility during growth, focus must be placed on the biological control of peroxidase activities at the cell wall. This includes the synthesis and secretion of peroxidases, the supp...

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confidence: 86%

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Role of Apoplastic and Cell-Wall Peroxidases on the Stimulation of Root Elongation by Ascorbate

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“…The region of ROS accumulation in K ϩ -starved roots was similar to the region where antioxidants such as ascorbate and dehydroascorbate accumulated in onion roots under control conditions (44). Increased ascorbate free radicals in this specific region were demonstrated to increase the uptake of sucrose, glucose, and nitrate in onion roots (45). In another study, (46) oxygen-free radicals in Arabidopsis roots were shown to cause a transient increase in K ϩ efflux.…”

Section: Discussionmentioning

confidence: 59%

Hydrogen peroxide mediates plant root cell response to nutrient deprivation

Shin

Schachtman

2004

Proc. Natl. Acad. Sci. U.S.A.

537

480

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Potassium (K ؉ ) is an essential nutrient required by plants in large quantities, but changes in soil concentrations may limit K ؉ acquisition by roots. It is not known how plant root cells sense or signal the changes that occur after the onset of K ؉ deficiency. Changes in the kinetics of Rb ؉ uptake in Arabidopsis roots occur within 6 h after K ؉ deprivation. Reactive oxygen species (ROS) and ethylene increased when the plants were deprived of K ؉ . ROS accumulated in a discrete region of roots that has been shown to be active in K ؉ uptake and translocation. Suppression of an NADPH oxidase in Arabidopsis (rhd2), which is involved in ROS production, prevented the up-regulation of genes that are normally induced by K ؉ deficiency, but the induction of high-affinity K ؉ transport activity was unchanged. Application of H2O2 restored the expression of genes induced by K ؉ deficiency in rhd2 and was also sufficient to induce high-affinity K ؉ transport activity in roots grown under K ؉ -sufficient conditions. ROS production is an early root response to K ؉ deficiency that modulates gene expression and physiological changes in the kinetics of K ؉ uptake.is essential to and required in large quantities by plants. To ensure the adequate supply, plants have a number of redundant mechanisms for K ϩ acquisition and translocation (1-3). Whereas much is known about K ϩ transport mechanisms, little is known about how plant cells sense and respond to changes in the K ϩ concentrations encountered in their environment. At the whole-plant level, K ϩ deficiency is known to enhance root respiration (4). This response suggests a shift in plant metabolism required for mineral acquisition or compensation for increased stress. External K ϩ concentrations alter the kinetics of uptake, which may be due to allosteric regulation by internal changes in K ϩ concentrations (5). Specific proteins in the plasma membrane and tonoplast were shown to be produced in response to K ϩ deficiency, indicating the synthesis of new transport proteins (6-8). Whereas changes in respiration and membrane transport occur in response to K ϩ deficiency, the cell biological events that trigger these changes have not been elucidated.In Escherichia coli, some of the molecules involved in the sensing and signaling of K ϩ deficiency have been elucidated (9). KdpD is a sensor kinase that undergoes autophosphorylation and transfers a phosphoryl group to a response regulator KdpE (10). The response regulator controls the expression of an operon coding for the high-affinity K ϩ uptake system in E. coli. The sensor kinase is thought to transduce changes in turgor caused by low K ϩ (11). It is not clear whether similar mechanisms are involved in transducing K ϩ deprivation in plants.Roots are the primary organs involved in mineral acquisition for plants and function at the interface with the rhizosphere. Although genes whose expression is related to external changes in nutrient composition have been identified, the cascade of cellular responses involved in sensing and si...

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“…The other hypothesis is that AAO causes the cytoplasm to expand. Monodehydroascorbic acid (MDHA) (a monooxidative species of AsA), which is considered to be the initial one-electron product of AAO activity (DHA forms by disproportionation of MDHA), could accept electrons from a plasma-membrane-bound cytochrome b. Membrane depolarization caused by transmembrane electron transport could stimulate plasma-membrane proton-pump activity (Gonzalez-Reyes et al 1994). Activation of the proton pump stimulates uptake of cellular nutrients and ions.…”

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Expansion of transgenic tobacco protoplasts expressing pumpkin ascorbate oxidase is more rapid than that of wild-type protoplasts

Kato

Esaka

2000

Planta

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When pumpkin (Cucurbita spp., cv. Ebisu Nankin) ascorbate oxidase cDNA was introduced into cultured cells of tobacco BY-2 (Nicotiana tabacum L. cv. Bright Yellow No. 2) by Agrobacterium-mediated transformation, the transgenic cells expressed and secreted the recombinant pumpkin ascorbate oxidase into the culture medium. These transgenic cells showed no morphological difference from wild-type cells. However, in the presence of applied hormones protoplasts prepared from the transgenic cells elongated more rapidly than those of wild-type cells. We propose that ascorbate oxidase may play a key role in the regulation of cell expansion perhaps by controlling transport processes through the plasma membrane, but not by affecting the cell wall.

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Nutrient Uptake Changes in Ascorbate Free Radical-Stimulated Onion Roots

Cited by 49 publications

References 17 publications

Role of Apoplastic and Cell-Wall Peroxidases on the Stimulation of Root Elongation by Ascorbate

Role of Apoplastic and Cell-Wall Peroxidases on the Stimulation of Root Elongation by Ascorbate

Hydrogen peroxide mediates plant root cell response to nutrient deprivation

Expansion of transgenic tobacco protoplasts expressing pumpkin ascorbate oxidase is more rapid than that of wild-type protoplasts

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